Journal of Neuroscience, Vol 5, 515-531, Copyright © 1985 by Society for Neuroscience
Phase and amplitude computations in the midbrain of an electric fish: intracellular studies of neurons participating in the jamming avoidance response of Eigenmannia
W Heiligenberg and G Rose
Electric fish monitor modulations in sensory feedback from their own
electric organ discharges (EODs) to locate moving objects and to detect
interfering EODs of their neighbors. The gymnotoid genus Eigenmannia
minimizes detrimental effects of jamming by EODs of its neighbors by
shifting its own EOD frequency away from a neighbor's EOD frequency that is
too close to its own. Since the animal lowers its own frequency if its
neighbor's frequency is higher and raises its frequency if its neighbor's
frequency is lower, this jamming avoidance response (JAR) requires that the
animal determine the sign of the difference frequency, Df, between the
interfering EODs. Eigenmannia obtains this information by evaluating
modulations in the amplitude and phase which its nearly sinusoidal EOD
signal experiences due to the interference with the neighbor's EODs. The
necessary logical operations are executed in the dorsal torus
semicircularis, an analogue of the inferior colliculus of higher
vertebrates, and are similar to operations underlying directional hearing.
By intracellular labeling of physiologically identified cells we have
identified the anatomy and functional characteristics of neurons involved
in the processing of amplitude and phase information. The JAR is controlled
by hierarchical and parallel processing of information in several laminae
of somatotopically ordered neurons. Phase differences between signals
received by electroreceptors in different parts of the body surface are
computed in lamina 6. Information about differential phase is then relayed
to multipolar cells in the deeper laminae 8, b and c, which also receive
information about modulations in local signal amplitude. These cells are
excited by a rise or fall of amplitude as well as by a lead or lag of
phase. According to their responses to either of these two variables, these
neurons can be divided into four classes. These classes encode all
information necessary for the control of the JAR and project to the optic
tectum. Dynamic properties and sensory specificities of the JAR are not
found in individual, properly tuned neurons but rather emerge statistically
from the joint effects of a large population of imprecisely tuned neurons.
This system is characterized by a distributed pattern of organization and
by the absence of a small number of key neurons whose malfunction would
jeopardize the behavioral response. The complexity of this neural machinery
appears unnecessary for the logically simple task of the JAR, and it
suggests that this behavior was acquired later in evolution by being
derived from more general motor responses to moving objects.(ABSTRACT
TRUNCATED AT 400 WORDS)
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